Bulletin of Insectology 65 (1): 149-160, 2012
ISSN 1721-8861
A review of the invasion of Drosophila suzukii in Europe and
a draft research agenda for integrated pest management
Alessandro CINI1,2, Claudio IORIATTI1, Gianfranco ANFORA1
1
Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’Adige (TN), Italy
2
Laboratoire Ecologie & Evolution UMR 7625, Université Pierre et Marie Curie, Paris, France
Abstract
The vinegar fly Drosophila suzukii (Matsumura) (Diptera Drosophilidae), spotted wing drosophila, is a highly polyphagous invasive pest endemic to South East Asia, which has recently invaded western countries. Its serrated ovipositor allows this fly to lay
eggs on and damage unwounded ripening fruits, thus heavily threatening fruit production. D. suzukii is spreading rapidly and economic losses are severe, thus it is rapidly becoming a pest of great concern. This paper reviews the existing knowledge on the pest
life history and updates its current distribution across Europe. D. suzukii presence has now been reported in nine European countries. Nonetheless, several knowledge gaps about this pest still exist and no efficient monitoring tools have been developed yet.
This review is aimed at highlighting the possible research approach which may hopefully provide management solutions to the
expanding challenge that D. suzukii poses to European fruit production.
Key words: spotted wing drosophila, cherry fruit fly, invasive species, berry fruit, insect control.
A new pest is threatening European fruit production
On the 2nd of December 2011 about 180 people attended
the international meeting “Drosophila suzukii: new
threat for European fruit production” in Trento. The
meeting represented a unique occasion to exchange information about the spread and impact of Drosophila
suzukii (Matsumura) (Diptera Drosophilidae), a new
fruit pest which is invading Europe. Researchers, producers, representatives of local institutions and phytosanitary services from ten European countries attended
the meeting, shared ideas, identified needs and tried to
elaborate strategies for the near future. The fly D. suzukii (also known as spotted wing drosophila, SWD, in
the USA) is an invasive pest endemic to South East Asia
which recently invaded western countries where it is
now threatening both the European and the American
fruit industry, due to its egg laying and feeding on unwounded ripening fruits of many plant species.
D. suzukii has been reported so far in most of the
Mediterranean countries in Europe and is rapidly
spreading toward north and east. In most attacked countries D. suzukii caused extensive economic damage to
small fruits (Goodhue et al., 2011); for this reason, and
because efficient monitoring and control tools are not
yet available for this species, growers and producers at
the Trento meeting pushed for immediate and efficient
solutions. The European and Mediterranean Plant Protection Organization (EPPO) recently presented a pest
risk assessment (PRA), in which it was concluded that
D. suzukii is a threat for most parts of the EPPO region,
where the pest will likely spread further, and that complete eradication is unfeasible and management difficult
(information available at www.eppo.org).
Inspired by the meeting, we review the knowledge
gained so far about D. suzukii life history traits in a
European context. Extensive information can be found
in Kanzawa (1935; 1936; 1939), while more recent biological data in English are available in Walsh et al.
(2011) and Lee et al. (2011b). We then provide an updated overview of its distribution across Europe. The
understanding of basic biology, ecology and distribution
is crucial for development of efficient management
strategies. The presence of multiple gaps in the present
knowledge was indeed clear in the aforementioned
meeting, and only an integrated and multidisciplinary
approach can face the challenge of understanding and
ultimately controlling this pest. Efficient and rapid solutions will only arise from a coordinated network of diverse expertises, from molecular biology and neurophysiology to pest management techniques. The main
focus of this review will thus be the possible research
lines able to provide management solutions to the challenge D. suzukii poses to European fruit production. We
draw up a draft research agenda in the hope that it will
guide future research.
Where does the pest come from and where
will it go?
What does D. suzukii look like?
D. suzukii adults are drosophilid flies (2-3 mm long)
with red eyes, a pale brown or yellowish brown thorax
and black stripes on the abdomen. Sexual dimorphism is
evident: males display a dark spot on the leading top
edge of each wing and females possess a large serrated
ovipositor (Kanzawa, 1939; Walsh et al., 2011). Despite
these evident features, the identification of D. suzukii
presents several challenges: adults can be easily misidentified, as it occurred for example in California,
where it was initially erroneously identified as Drosophila biarmipes Malloch (Hauser, 2011).
The distinguishing features of the two sexes (serrated
ovipositor and black wing spots) are present in other
Drosophila species, thus making species identification
difficult in areas where they are sympatric. For example,
Drosophila subpulchrella Takamori et Watabe males’
black spots are very similar in shape and position to
those of D. suzukii (Takamori et al., 2006). Moreover,
small or young D. suzukii males sometimes lack the
wing spot, which becomes clearly visible circa two days
after emergence (Hauser, 2011), which could lead to
misidentification with other Drosophila males. Other
characteristics may thus guide identification, such as the
sex combs on the foretarsi (D. suzukii has one row of
combs on the first and one row on the second tarsal segment) (Kikkawa and Peng, 1938; Parshad and Paika,
1965; Bock and Wheeler, 1972). Therefore, in many
cases, only analyses of a full set of features, also including male genitalia (Hsu, 1949; Okada, 1954; Parshad and Paika, 1965; Bock and Wheeler, 1972), enable
a reliable identification. Similar problems arise with
females. On the basis of the shape and length of the
ovipositor, D. suzukii can be easily discriminated from
related species, as for example D. biarmipes, but not
easily from other species such as Drosophila immigrans Sturtevant and D. subpulchrella (Takamori et al.,
2006) which possess very similar ovipositors (Hauser,
2011). In such cases, a final determination should rely
on the relative size of spermatheca compared to ovipositor’s size: it is thus feasible only for the trained
eyes of taxonomists (Hauser, 2011). The situation is
complex also for immature stages (eggs, larvae and pupae), where no reliable morphological diagnostic features have been identified (Okada, 1968). The D. suzukii egg has two respiratory appendages but this character is not species-specific. Therefore, DNA barcoding
is the only fully reliable identification tool (Doczkal D.,
http://barcodenews.net/2012/02/22/).
A difficult tree for a fruit pest
D. suzukii belongs to the subgenus Sophophora, which
is divided into several species groups. One of them, the
melanogaster species group, also contains the famous
“workhorse” of experimental biology and genetics,
Drosophila melanogaster Meigen (Powell, 1997). The
melanogaster group is further divided into species subgroups, one of which (the suzukii subgroup) composes,
together with 6 other subgroups, the “oriental lineage”
(Kopp and True, 2002; Schawaroch, 2002; van der
Linde et al., 2010).
However, relationships between and within these subgroups are still far from being resolved, and the suzukii
subgroup itself is commonly regarded as polyphyletic
(Kopp and True, 2002). A recent paper suggested
D. biarmipes as the sister species of D. suzukii (Yang et
al., 2011), in accordance with previous findings (Kopp
and True, 2002; Barmina and Kopp, 2007), but in contrast with Prud’homme et al. (2006) and van der Linde
and Houle (2008), which instead supported D. subpulchrella as the sister species of D. suzukii (with D. biarmipes being the sister species of D. subpulchrella +
D. suzukii). Conflicting results could be due to inadequate sampling of taxa and characters, as well as being
due to the complex phylogenetic signal residing in different genes (Rota Stabelli, unpublished data).
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D. suzukii is rapidly spreading across Europe
If phylogenetic relationships of D. suzukii have not
been resolved yet, little is known about its geographical
origin either. It was firstly described in Japan in 1916,
where it was found to attack cherries, but it is still uncertain whether it is native to this area or possibly introduced around the turn of the last century (Kanzawa,
1936). The fly is also present in the eastern part of
China (Peng, 1937), Taiwan (Lin et al., 1977), North
and South Korea (Chung, 1955; Kang and Moon, 1968),
Pakistan (Amin ud Din et al., 2005), Myanmar (Toda,
1991), Thailand (Okada, 1976), the Russian Far East
(Sidorenko, 1992) and India (Kashmir region, Parshad
and Duggal, 1965), where it was described as the D. suzukii subspecies indicus (Parshad and Paika, 1965).
D. suzukii is currently spreading in many areas, such
as the USA (West and East coast), Canada, Mexico and
Europe (a history of the introduction in North America
is reviewed by Hauser, 2011). A key feature of its rapid
spread was the initial lack of regulation over the spread
of any Drosophila. In Europe it was first reported in autumn 2008 in Spain (Rasquera Province) (Calabria et
al., 2012), although a recent publication offers an update of its first findings in Europe. Malaise traps deployed in Tuscany (San Giuliano Terme, Pisa, Italy) in
2008, whose catches were examined only recently,
caught D. suzukii adults contemporaneously with those
deployed in Spain (Raspi et al., 2011).
In 2009 D. suzukii adults were recorded in traps in
other regions of Spain (Bellaterra, near Barcelona)
France (Montpellier and Maritimes Alpes) and Italy
(Trentino) (Grassi et al., 2009; Calabria et al., 2012). In
Trentino, both first oviposition on wild hosts (Vaccinium, Fragaria and Rubus spp.) and economically important damage on several species of cultivated berries
were reported (Grassi et al., 2009).
By 2010-2011, the range of D. suzukii was further
enlarged. In Italy it was reported in several other regions: Piedmont, Aosta Valley, Lombardy, Veneto,
Emilia Romagna, Liguria, Marche and Campania (Franchi and Barani, 2011; Pansa et al., 2011; Süss and Costanzi, 2011; Griffo et al., 2012) and in France it was
found from Corsica up to Ile de France (Mandrin et al.,
2010; Weydert and Bourgouin, 2011). Then, many other
European countries made their first record: Switzerland
(Baroffio and Fisher, 2011), Slovenjia (Seljiak, 2011),
Croazia (Masten Milek et al., 2011), Austria (Lethmayer, 2011), Germany (Vogt et al., 2012) and Belgium
(EPPO Website).
The data presented and summarized in figure 1 reflect
the current known distribution of D. suzukii in Europe.
It appears to be spreading rapidly and all of continental
Europe is at risk for invasion. We advocate an integrated, precise and area-wide monitoring network. It is
worthwhile to note that the lack of reports from several
areas is probably due to a lack of monitoring rather than
to an actual absence of D. suzukii. Thus, the history of
reports might reflect differences in the sampling effort
and/or problems of awareness rather than the true D.
suzukii distribution.
Considering the recent reports together with the outputs of the available degree-day phenological models
Figure 1. The escalating outbreak of D. suzukii in Europe. European countries and Italian regions are represented by
different colours on the maps according to the year of the first finding. The fly drawings are placed in the areas of
the first record.
(Damus, 2009; Coop, 2010) and analysis of D. suzukii
host plants distribution (EPPO website), it is very likely
that D. suzukii will spread all over Europe. Indeed, ecological simulations indicate the northern humid areas as
more suitable ecosystems compared to the Mediterranean drier environments, especially because desiccation
seems to be a limiting factor for drosophilids (Walsh et
al., 2011). If the current climate changes are taken into
account, even Scandinavian countries can not be considered exempt from these risks of invasion. On a wider
geographic perspective, according to D. suzukii biology,
the global expansion in regions with climatic conditions
spanning from subtropical to continental is highly likely
to happen (Walsh et al., 2011). Furthermore, niche
shifts, as occurred for other pests (e.g. Zaprionus indianus Gupta, Da Mata et al., 2010), should not be excluded (Calabria et al., 2012), which suggests that
D. suzukii could become a global problem for fruit production. It has yet to arrive in South America or Africa,
but seems likely to reach there in the future.
Why is D. suzukii a threat for fruit production?
Unlike most other Drosophilidae, possibly exempting
D. subpulchrella, D. suzukii is able to lay eggs in
healthy, unwounded fruit thanks to the serrated female
ovipositor and not only on damaged or overripe fruits
(Sasaki and Sato, 1995). Hence, ripening fruits are preferred over overripe ones (Mitsui et al., 2006).
Most damage caused by D. suzukii is due to larvae
feeding on fruit flesh, however the insertion of the
prominent ovipositor into the skin of the fruit can cause
physical damage to the fruit, as it provides access to sec-
ondary infections of pathogens - such as filamentous
fungi, yeasts and bacteria - that may cause faster deterioration and further losses. Additional costs are related to
increased production costs related to pest control (monitoring and chemical input costs, increased labour and fruit
selection, reduction of the fruit shelf life, storage costs)
and to the decrease of foreign market appeal for production from contaminated areas (Goodhue et al., 2011).
However, the oviposition habit itself is not enough to
explain the dramatic impact of D. suzukii on production.
In the next sections we show the main features making
D. suzukii a threat of high concern for the European
fruit production.
Extreme fecundity
Adults of D. suzukii reach maturity one or two days
after emergence (during the warm season). Mating occurs from the first days of life and females start to lay
eggs already from the second day from emergence. Females typically lay 1-3 eggs per fruit in up to 7-16 fruits
per day; since they are able to oviposit for 10-59 days,
they can lay up to a total of 600 eggs during their lifetime (around 400 eggs on average). Eggs hatch within 2
to 72 hours after being laid inside fruits, and larvae mature (inside the fruit) in 3 to 13 days. Pupae reside inside
or, less frequently, outside the fruit, for 3 to 15 days.
Depending on the temperature, a minimum of 8 days is
required from oviposition to adult emergence. This very
short generation time implies that D. suzukii can complete several generations in a single cropping cycle and
up to 7 to 15 generations in a year, according to the specific climatic conditions, thus allowing an explosive
population growth (life-cycle details can be found in
Kanzawa, 1939; Mitsui et al., 2006; Walsh et al., 2011).
151
Tolerance of a wide range of climatic conditions
The ability to survive and reproduce in a wide range
of climatic conditions is obviously a relevant factor for
insects. Limiting temperatures for D. suzukii reproduction are between 10 and 32 °C for oviposition and up to
30 °C for male fertility (Sakai et al., 2005). The peak of
activity and development is around 20 to 25 °C (Kanzawa, 1939). D. suzukii can thus be considered a species with high thermal tolerance, being both heat tolerant (viable D. suzukii populations resist to the hot
summers in Spain) and cold tolerant (D. suzukii is present in cold areas, such as mountain regions in Japan
and Alpine areas).
Adults are particularly tolerant to cold compared to
other drosophilids (Kimura, 1988) and mated females in
reproductive diapause are considered to be the overwintering stage of D. suzukii (Kanzawa, 1939; Mitsui et al.,
2010; Walsh et al., 2011). Whether this tolerance is
physiological or mediated by behavioural adaptation is
still unclear and several authors suggest that D. suzukii
survival under harsh conditions might be increased by
altitudinal migration (Mitsui et al., 2010), acclimatization (Walsh et al., 2011) and/or overwintering in manmade habitats or other sheltered sites (Kimura, 2004).
Wide host range
D. suzukii is able to develop on a very wide range of
both cultivated and wild soft-skinned fruits with many
host plants in the native and in the invaded areas, with
berries being the preferred hosts. The following list of
D. suzukii host plants grouped based on botanical family
should be still considered tentative, since some information is not well documented: Rosaceae - Fragaria
ananassa (strawberry), Rubus idaeus (raspberry), Rubus
fruticosus, Rubus laciniatus, Rubus armeniacus and
other Rubus species and hybrids of the blackberry
group, Rubus ursinus (marionberry), Prunus avium
(sweet cherry), Prunus armeniaca (apricot), Prunus
persica (peach), Prunus domestica (plum), Eriobotrya
japonica (loquat); Ericaceae - Vaccinium species and
hybrids of the blueberry group; Grossulariaceae - Ribes
species including the cultivated currants; Moraceae Ficus carica (fig), Morus spp. (mulberry); Rhamnaceae
- Rhamnus alpina ssp. fallax, Rhamnus frangula (buckthorn); Cornaceae - Cornus spp. (dogwood); Actinidiaceae - Actinidia arguta (hardy kiwi); Ebenaceae Diospyros kaki (persimmon); Myrtaceae - Eugenia
uniflora (Surinam cherry); Rutaceae - Murraya paniculata (orange jasmine); Myricaceae - Myrica rubra (Chinese bayberry); Caprifoliaceae - Lonicera spp. (honeysuckle); Elaeagnaceae - Elaeagnus spp.; Adoxaceae Sambucus nigra (black elder); Vitaceae - Vitis vinifera,
Vitis labrusca (Kanzawa, 1939; Grassi et al., 2011; Lee
et al., 2011b; Seljak, 2011; Walsh et al., 2011). However, current data suggest that host preference is heavily
dependent upon the local abundance of hosts.
The V. vinifera case is still matter of verification. Despite laboratory experiments that showed a significantly
lower oviposition susceptibility and developmental rate
of D. suzukii on grapes than on berries and cherry (Lee
et al., 2011a), recent observations in vineyards in
Northern Italy would indicate that V. vinifera can be152
come a field host (with soft skinned varieties being
more impacted) (Griffo et al., 2012).
The host-choice flexibility of D. suzukii is also demonstrated by the ability to develop also on tomato under
laboratory conditions (not recorded so far as a host in
the field, even if D. suzukii adults have been trapped in
tomato crops in France (EPPO website).
The wide host range represents a pest management
constraint not only because D. suzukii can cause damage
to many species, but also because populations can survive almost everywhere, alternating hosts with different
ripening times through the year, both cultivated and
wild. Indeed, crop plants, usually cultivated in high density monoculture, allow rapid and impressive population
growth, while wild hosts and ornamental plants may
serve as refuges from management treatments, and provide later re-infestation sources and overwintering habitats (Klick et al., 2012).
The wide host range and the ability to damage thick
ripening fruits, gives to D. suzukii a wide but at the
same time specialized ecological niche. However, overlapping niches and possible competition with other drosophilids needs to be investigated.
High dispersal potential
D. suzukii has a high dispersal potential (Hauser,
2011; Calabria et al., 2012), which would seem to be
confirmed by its rapid spread in invaded countries and
its presence on several continents, as well as remote islands (i.e. Hawaii; Kaneshiro, 1983;). Passive diffusion
due to global trade is likely the main cause of the spread
of D. suzukii, as for many other invasive species (Westphal et al., 2008). The apparently intact and healthy
status (before larval activity) of the fruits infested with
D. suzukii is likely to compound the problem, as it increases the risk that infestation will remain undetected
and thus the risk of passive dissemination of D. suzukii
(Calabria et al., 2012).
A research agenda for integrated pest management
Estimating the costs associated with D. suzukii impact is
a complex task, with several factors (direct and indirect
costs) that must be taken into account, their interdependency and the dynamic nature of the system (Goodhue
et al., 2011; Walsh et al., 2011). Preliminary studies in
the USA indicate an annual loss of more than 500 million dollars in five affected crops (strawberries, blueberries, raspberries, blackberries and cherries) in three
states (California, Oregon and Washington) (Bolda et
al., 2010). Because of regional monoculture, economical losses might be even larger in proportion at a local
scale. A preliminary study estimated that Trento province (Northern Italy), the area devoted to small fruit cultivation (about 400 hectares) faced a loss around
500,000 € in 2010 and 3 million € in 2011 (Ioriatti et
al., 2011).
While fast answers to D. suzukii could be provided by
changes in the pesticide regulations and by sanitation
procedures, these management techniques will only
have short-term application and effects. Solutions that
are effective and sustainable over the long term are hard
to find in the absence of detailed knowledge of the pest
species life history, as well as of its biological attributes
and population dynamics. Research on fundamental aspects is thus a key step enabling future management solutions.
Below we propose a research agenda, which identifies
the main relevant topics we consider to be fundamental.
The research agenda is based on a paradigm we called
the “3M framework”, which stands for Monitoring,
Modelling and Managing. These steps should be tightly
interconnected to each other in order to properly face a
pest invasion challenge; however, for clarity, we will
treat them separately in this review.
Monitoring
A reliable monitoring of the pest presence is the first
step for a successful integrated pest management (IPM).
So far, the monitoring of D. suzukii has been based on
trapping methods available for other pests and for Drosophilidae in general, i.e. fermentation baits and vinegar, with the main baits being represented by one or a
mix of the following substances: ripe bananas, strawberry puree, cherry juice, citronella oil, geranium oil,
apple cider, vinegar, cherry wine, sugar and yeast mixtures (Wu et al., 2007; Walsh et al., 2011). A recent
study showed a high level of attraction to a combination
of vinegar and wine, possibly due to a synergistic effect
of acetic acid, ethanol and other vinegar/wine volatiles
(Landolt et al., 2012).
While D. melanogaster and other drosophilids can
complete all life stages on the same fermenting materials, gravid D. suzukii females need to find undamaged
ripening fruits for oviposition. It is therefore likely that
the odour produced by fermenting fruits represents a
generic food cue to D. suzukii, whereas egg-laying females target volatiles from fresh fruits specifically. Unfortunately, the knowledge of the sensory and chemical
ecology of D. suzukii in relation to feeding, mating and
oviposition is still extremely poor. In particular, the
identification of the most behaviourally-active volatiles
emitted by fruits host of D. suzukii might allow the development of more selective and powerful attractant
lures that could be released at controlled rates from dispensers. Knowledge of kairomones for D. suzukii will
also form the basis of environmentally friendly strategies, such as mass trapping and attract and kill, which
showed promising results in initial studies (Kanzawa,
1934; Wu et al., 2007).
The trapping performance is also highly influenced by
the trap’s colour, shape and structure. Red and black
have been shown to be the most attractive colours,
hence coloured traps would be recommended (Mitsui et
al., 2006; Edwards et al., 2012). The most currently
used traps are plastic bottles or cups with multiple small
lateral holes (diameter between 5-10 mm) containing
the liquid bait. The addition of a small drop of surfactant or the placement of sticky cards inside the trap increases trapping efficiency by preventing the escape of
flies (Walsh et al., 2011). Even though some trapping
protocols already exist (e.g. Dreves et al., 2009), a
really highly performing and species-specific trap has
not been developed yet (Walsh et al., 2011). Further research on baits, trap design and trapping protocols is
thus needed.
In addition to optimizing bait (with single or multiple
components), trap shape, and colour, it is also important
to study the effects of trap placement both in terms of
space and time. Traps are currently either placed on the
ground or hung on plants near fruits, and preliminary
evidence indicates that traps perform best when placed
in cool and shaded areas (Walsh et al., 2011). Future
research should investigate the importance of spatial
variables, both on the microscale (e.g. height, on plants
or on the ground) and on the mesoscale (e.g. inside crop
areas or along the boarders), as well as the importance
of the timing of trapping. Here, e.g., mass trapping
could be more effective at the onset of the season than
later on, when the population has already reached high
densities.
Modelling
Understanding ecological factors influencing feeding,
survival, and reproduction is crucial in order to understand and forecast the current and future distribution and
population dynamics of D. suzukii. Attention should be
paid to both the spatial (distribution at large and small
scales) and temporal scale (seasonal variation in abundance). Coupling high resolution techniques (such as
georeferencing) with basic biological knowledge (e.g.
life cycle, life history traits) will allow the prediction of
the fine scale distribution, pest pressure maps and degree day models, allowing reliable estimates of D. suzukii impact and economic losses. This will improve the
choices in sanitation, management and socioeconomical procedures, and, as a consequence, improve
the effectiveness of pest management decisions.
A landscape ecology approach would also be crucial
to understand the movement of D. suzukii across the
landscape, highlighting possible refuge areas as well as
potential sources of re-infestation (Ohrn and Dreves,
2012). Modelling should also tackle the timing of
D. suzukii population growth, starting from the first seasonal re-infestations to forecast the seasonal dynamics.
This could help in understanding when to set the trap
and deliver the chemical treatments. Degree-day models
are currently being developed (Damus, 2009; Coop,
2010), but future research will result in more precise
and specific models.
The interactions between D. suzukii and the several
host plants should be taken carefully into account. This
step could be facilitated by the availability of
phenological models for many host species. However it
may also be hindered by the great number of D. suzukii
hosts. It is thus imperative to deepen our understanding
of D. suzukii-host plant interactions and dynamics.
Therefore, research should investigate host preference
and the factors affecting D. suzukii choice of oviposition
and feeding sites, such as local abundance, population
history or prior experience. Interesting insights in this
regard could be gathered through the study of D. suzukii
biology in its native range, where such phytophagousplant interactions evolved. Initial laboratory experi153
ments indicate that, while D. suzukii could show preferences toward certain host plants in nature, it could also
show differences in the breeding success and thus in the
level of impact on different hosts (Lee et al., 2011a).
The mechanisms of host reactions and differences in
their susceptibility (among species, among varieties and
across landscape and times) will thus be worth of investigating. The integration of crop phenology, pest life cycle and host-pest interactions will allow the prediction
of spread and impact.
Managing
Preventing new introduction and
re-infestation
D. suzukii is spreading across Europe and eradication
and containment do not seem feasible (EPPO website).
However, in order to keep D. suzukii populations at a
manageable level, it is critical to avoid recurrent introductions and re-infestations.
From this perspective, it is crucial to understand
where the pest comes from, by which vectors it has been
and is still being introduced, and determine the most
likely sources of re-introduction in a certain region and
re-infestation of a specific crop area. International trade
is considered a key factor increasing the likelihood of
biological invasion (Westphal et al., 2008) and undetected infested fruits are believed to be the most likely
pathway of colonization for D. suzukii (EPPO website).
Through population genetics it would be possible to disclose D. suzukii colonization patterns and dynamics
(e.g. Fernandez Iriarte et al., 2009 for a related species)
and to trace the routes of invasion, which could allow
prevention of recurrent introductions. Based on preliminary genetic results and on the similarities between the
dates of introduction, Calabria et al. (2012) suggested
that the D. suzukii invasions in North America and in
Europe could be related.
Removing any possible source of D. suzukii either
outside (wild hosts, sites in neighbouring grower fields
and ornamental plants in backyard gardens) or inside the
orchard (fruit production waste) is crucial in order to
prevent re-infestations on local scale, and thus represents a key step in IPM (Walsh et al., 2011). Any fruit
that remains in the crop can be a food source or a breeding site for D. suzukii, thus acting as a potential reinfestation source. However, once removed, fruits must
be destroyed. Several widely used techniques, e.g. composting could in fact worsen the problem, since the
fruits and the larvae are not rapidly destroyed, but rather
are able to develop rapidly in the warm environment
produced by decomposition processes. Several options
for effective disposal of potentially contaminated fruit
material have been proposed, e.g. solarization, insecticide treatment, disposal in closed containers, crushing,
cold treatment, bagging and burial (Walsh et al., 2011;
EPPO website). These sanitation procedures should be
widely applied in the affected areas, in order to avoid
the persistence of neglected re-infestation sources.
Therefore, many local entities officially imposed sanitation measures to growers. Research is underway for the
evaluation of other management methods based on
physical barriers. As an example, in Japan it was dem154
onstrated that covering plants with netting (0.98 mm
mesh size) fully prevented the D. suzukii infestations
(Kawase et al., 2007).
Chemical control
Current control efforts for D. suzukii rely heavily on
the use of insecticides. Unfortunately, the insecticides
which are currently available to growers for control of
D. suzukii are not very effective, since the use of highly
efficient broad spectrum chemicals is being progressively restricted. In particular, organic production is seriously threatened because only few natural insecticides
are admitted and their efficacy against D. suzukii is either not known or lower than the conventional insecticides (Walsh et al., 2011). Furthermore, the fast generation turnover requires many chemical interventions at
the ripening stage, which can increase the risk of residues in fruits, promote insect resistance and negatively
affect pollinators and other beneficial species.
However, due to the lack of specific insecticides
against D. suzukii larvae within fruits, research has been
focused on treatments based on chemicals targeting
adults. Kanzawa (1939) found that camphor oil was the
most effective of the treatments he employed, followed
by nicotine sulphate, kerosene emulsion, and neoton but
no treatment totally prevented oviposition and most of
these materials are no longer used or acceptable. Recent
laboratory and field studies both in the USA and in EU
revealed that among the registered insecticides organophosphates, timely applications of pyrethrins and spinosyns can provide good contact activity and residual impact for up to 12-14 days (Beers et al., 2011; Bruck et
al., 2011; Profaizer et al., 2012). In contrast, the efficacy of the neonicotinoids as adulticides was not satisfactory (Bruck et al., 2011).
Initial trials in the Trentino Province indicated that
only lambda-cyhalothrin provided an adequate level of
control. However, at high population densities repeated
applications by alternating pyrethrins and spinosad in
strawberry plantations only reduced the damage immediately after the treatment and had negligible impact at
the end of the harvest time (Grassi et al., 2012). Therefore, future research needs to address not only identification of effective chemicals, but must also consider
how protocols for delivery of chemicals can be optimized. In addition, growers should undertake a pesticide
rotation, in order to avoid or at least delay the evolution
of insecticide resistance, which can be easy in Drosophila species (even associated with a single resistance
allele, see Ffrench-Constant and Roush, 1991) also
thanks to the numerous generations per year.
Control strategies based on interferences with communication
Among the environmentally safe strategies those
based on the interferences with the insect communication, both intra- and inter-specific, are often the most
effective and enduring ones (i.e. mating disruption, attract and kill, mass trapping). These approaches act either by reducing the population survival (attract and kill,
mass trapping) and/or by interfering with its reproduction (mating disruption).
Although more research is needed to decipher the sexual communication of D. suzukii, advantage could be
taken from the vast knowledge on the model organism
D. melanogaster. Drosophila species use aggregation
pheromones which often act in synergism with food
odours (Bartelt et al., 1985). It might be speculated that
D. suzukii releases also cuticular hydrocarbons which
act as sex pheromones for a short range attraction (Antony and Jallon, 1982).
In addition, both visual cues and air-borne sounds
emitted by wing vibrations have been demonstrated to
play a role in the short-range courtship of D. suzukii
(Ewing, 1978; Fuyama, 1979). Similarly to D. melanogaster, sex peptides produced in the D. suzukii male accessory glands and transferred into the female during
copulation were shown to suppress the female receptivity and to stimulate oviposition (Ohashi et al., 1991;
Schmidt et al., 1993).
Whether the D. suzukii mating and oviposition behaviour is susceptible to be disrupted with affordable and
effective methods based on synthetic pheromones, on
mechanical signals (i.e. vibrational mating disruption;
Eriksson et al., 2012), or by combinations of them is
still matter of conjecture, but is a promising area for future research.
Biological control
There are multiple biocontrol agents (fungi, bacteria,
viruses and other natural enemies of the pest, such as
predators and parasitoids) that could be employed in
IPM for D. suzukii.
Biocontrol activity of microorganisms:
Recently, DNA viruses have been isolated also in
Drosophila species (Unkless, 2011) and were found to
be related to other viruses used for pest control. These
findings open the way for the evaluation of control of
D. suzukii based on viral pathogens and research is urgently needed on this subject.
Parasitoids:
Research on arthropods as biocontrol agents is also
urgently needed, although a control approach based on
arthropod natural enemies would probably be very difficult for a high-reproduction species like D. suzukii.
Nevertheless, several valuable studies on this topic have
been performed in Japan, in the native range of the species. Potentially, results from these studies could help
identify novel management strategies based on introduction and permanent establishment of natural enemies of
D. suzukii from its native range for a long-term control.
Early experiments tested the efficacy of Phaenopria
spp. (Hymenoptera Diapriidae) under laboratory conditions, however, results were unsatisfactory (Kanzawa,
1939). More recent studies have explored the occurrence and biology of several D. suzukii parasitoids in
Japan (Ideo et al., 2008; Mitsui et al., 2007; Kimura unpublished data). Species of the genus Ganaspis (Hymenoptera Figitidae) showed the highest rates of D. suzukii parasitism (ranging from about 2 to 7%). These
species lay eggs in larvae that are feeding in fruits and
exhibits a high level of specificity for D. suzukii. On the
other hand, Leptopilina japonica Novkovic et Kimura
(Hymenoptera Figitidae) and Asobara japonica Belokobylskij (Hymenoptera Braconidae) were able to attack larvae and pupae only in fallen decaying fruits and
attacked a wide range of drosophilid hosts (Mitsui and
Kimura, 2010; Kimura unpublished data).
However, it has been recently demonstrated that increased constitutive hemocyte levels involved in encapsulation of parasitoid eggs enable D. suzukii larvae to
produce a more vigorous immune response and resistance than D. melanogaster to their generalist parasitic
wasps (Kacsoh and Schlenke, 2012).
Nevertheless, another approach for the biological control of D. suzukii would be to enhance the effect of beneficial organisms already present in the newly invaded areas, generalist and widespread species having D. suzukii
in their host range or, otherwise, species able to adapt
their selection strategies to the invader. Indeed, Pachycrepoideus vindemmiae (Rondani) (Hymenoptera Pteromalidae), a generalist pupal parasitoid considered for a
long time as a major natural enemy of D. melanogaster
(Martelli, 1910), was recently found to be also associated
with D. suzukii in USA (Brown et al., 2011).
Two promising candidates are also Asobara tabida
Nees and its sibling species Asobara rufescens Foerster
(Hymenoptera Braconidae), which are the most common parasitoids of frugivorous drosophilids in Europe
(Vet et al., 1984) and shown able to develop on D. suzukii in the field in Japan (Mitsui et al., 2007). Likewise
and in accordance with observations in Japan, generalist
species of the genus Trichopria (Hymenoptera Diapriidae) distributed in US and EU are likely to accept D.
suzukii as an additional host (Kimura, personal communication). Furthermore, the impact on D. suzukii population of generalist predators, such as several Orius
(Rhynchota Anthocoridae) species, is under evaluation
in different laboratories.
Exploiting pest-endosymbionts associations:
A promising, but sometimes neglected method of reducing pest populations is the exploitation of the intimate association of the pest species with endosymbionts
(Zindel et al., 2011). Arthropods are frequently infected
with one or more micro-organisms which can have
beneficial, neutral or detrimental effects on their hosts.
These interactions may directly or indirectly influence
the population dynamics of many pest species and could
thus potentially be of great interest for agricultural pest
management (Zindel et al., 2011).
For example, the obligate intracellular bacteria of the
genus Wolbachia are estimated to infect more than half
of the living insect species, whose reproduction they are
able to manipulate by provoking several phenotypic effects (cytoplasmic incompatibility, induction of parthenogenesis, male killing and feminization) (Werren et al.,
2008; Zindel et al., 2011).
Cytoplasmic incompatibility (CI) is the most common
reproductive effect induced by Wolbachia in their hosts.
CI prevents infected males from successfully mating
with females with different Wolbachia infection status
(non-infected or infected with different and incompatible
strains) (Werren et al., 2008). Thus, CI could be used to
155
suppress insect pest populations in a manner analogous
to the sterile insect technique (SIT) by releasing males
carrying CI-inducing endosymbionts (see Zabalou et al.,
2004). Wolbachia inducing CI have been widely discovered in several Drosophilidae (reviewed in Werren et al.,
2008) and preliminary results suggest that also D. suzukii
is infected with Wolbachia (Siozios unpublished data).
However, Wolbachia has complex phenotypic effects on
its hosts, depending on strain, host genotype and interactions between them. In addition to CI, Wolbachia infection could have significant survival and fecundity effects
in drosophilids (Fry et al., 2004). It has recently been
discovered that Wolbachia infection enhances fertility in
Drosophila mauritiana Tsacas et David, with an average
four-fold increase in the egg laying rate of infected flies,
compared to uninfected individuals (Fast et al., 2011).
Future research should address the extremely high fecundity found in D. suzukii, in order to assess whether it
is linked in a similar way to Wolbachia infections. Finally, due to the rapid spread of Wolbachia in insect
population, these bacteria have also been suggested as
vectors for desirable genetic modification that could be
used in control efforts (Sinkins and Gould, 2006).
The control potential of Wolbachia is also related to the
natural enemies of the pest species. Indeed, Wolbachia
was shown to induce parthenogenesis in several hymenoptera parasitoids (Werren et al., 2008), thus suggesting
potential advantages in their rearing, releasing and efficacy. In addition, a fertility-enhancing effect similar to
that found in D. mauritiana, has been revealed in the
D. suzukii parasitoid A. tabida (Dedeine et al., 2001).
On the other hand, Spiroplasma bacteria can rescue
the sterilization effect induced by a nematode on Drosophila neotestacea Grimaldi, James et Jaenike (Jaenicke et al., 2010), while Wolbachia infections in
D. melanogaster flies reduce the impact of the fungal
pathogen Beauveria bassiana (Panteleev et al., 2007)
and of viruses (Werren et al., 2008). These three examples are of particular interests, since nematodes, fungal
pathogens and viruses are three widely used options for
biocontrol of pest insects and candidate biocontrol
agents for D. suzukii.
Other IPM strategies
Reducing pest population is also possible by inundative releases of sterile insects. The development of the
SIT represents a major breakthrough in pest management science (Vreysen et al., 2006). Indeed, SIT has
several advantages compared to other control strategies,
e.g. being safe to non-target organisms and acting with
an inverse density-dependent mechanism; in addition,
SIT could be integrated with other control strategies
(Vreysen et al., 2006). Therefore, the feasibility, procedures and possible drawbacks of SIT applied to D. suzukii management, with male sterility either induced by
irradiation or based on transgenic insect strains, should
be investigated, to promote successful use of SIT in the
management of several pest species (Dyck et al., 2005).
This would include a requirement for mass rearing of
high quality and competitive insects. The short generation time and large field populations would present a
challenge for control by SIT.
156
D. suzukii as a vector of plants
pathogens
An important topic to address is whether D. suzukii
could act as a vector of plant pathogens, thus provoking
additional damages to the attacked species. Indeed, Drosophila flies have long been recognised as microorganism
disseminators and the role of fungal disease vectoring has
been demonstrated for D. melanogaster, which carries
(both on its cuticle and inside its digestive tract) the fungus Botrytis cinerea (Louis et al., 1996). While D. melanogaster only attacks overripe/rotten fruits, thus limiting
the damage caused by B. cinerea, D. suzukii targets intact
fruits, making it possible for the fungus to penetrate inside. Research should thus investigate the potential of
D. suzukii as a carrier of other microbial diseases.
Indeed, a possible link between the D. suzukii spread
and the expansion of two host plants diseases (Monilinia
brown rots and Botrytis rots) in Slovenia has been suggested (Seljiak, personal communication). Interestingly,
also the occurrence of interactions between specific
yeast species associated with D. suzukii and the yeast
profile of the host fruits has recently been proposed,
which paves the way for another intriguing field of research on this pest (Hamby et al., 2011).
Taking advantage from a close
relative:
the
model
system
D. melanogaster
This review highlighted that knowledge about D. suzukii is still limited but great advantage could be taken
from the vast experience on the related excellent model
organism, D. melanogaster. Their close relationship offers also fascinating opportunities for addressing some
longstanding questions in the field of insect biology
with a practical outcome.
For instance, comparative research in D. melanogaster
will accelerate progress in improving the effectiveness
of insecticides. In addition, comparisons with D. melanogaster could shed light on the evolution of ecological
innovations (as shown in other drosophila flies, Dekker
et al., 2006) and help researchers in understanding what
makes a species invasive.
By harnessing the biology workhorse D. melanogaster,
as well as the high priority pest D. suzukii, the Drosophila genus will probably become a model also for agricultural and crop protection studies.
Conclusions
The rapid spread of the invasive fruit pest D. suzukii
poses a challenge to fruit production in Western countries. The biology of D. suzukii suggests that an effective control effort requires an area wide IPM program.
In order to accomplish this, research needs to address
D. suzukii basic biology, the development of management tools, the transfer of knowledge and technology to
users and, finally, the implementation of the IPM program also at a cultural and societal level (Lee et al.,
2011b; Dreves, 2011). While short term solutions to
limit the current dramatic damage are strongly needed,
only long-term and environmentally friendly manage-
ment approaches will allow a sustainable control of this
pest. To this aim, research should be carried out to shed
light on many knowledge gaps that are still present. The
future will surely see a great increase in the knowledge
of D. suzukii biology, impact and management.
Acknowledgements
The authors warmly thank all the speakers and participants of the D. suzukii meeting in Trento and the colleagues of “Fondazione Edmund Mach” for the enlightening discussions. We are grateful to R. Cervo for the
critical reading of an early version of the manuscript.
Thanks also to I. Pertot, O. Rota Stabelli, V. Mazzoni,
S. Siozios, J. Bengtsson and B. Mazza for the useful
comments and to Carlotta Cini and Flavia Evangelista
for the language revision. We thank Sabrina Pintus of
the “Ministero delle Politiche Agricole Alimentari e Forestali” (Italy) for her suggestions. The preparation of
the review was funded by Autonomous Province of
Trento, Call for Proposal Major Projects 2006, Project
ENVIROCHANGE.
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Authors’ addresses: Gianfranco ANFORA (corresponding
author, [email protected]), Claudio IORIATTI, Research and Innovation Centre, Fondazione Edmund Mach, via
Edmund Mach 1, 38010 San Michele all’Adige (TN), Italy;
Alessandro CINI, Laboratoire Ecologie & Evolution UMR
7625, Université Pierre et Marie Curie, 7 quai St Bernard,
75252 Paris, France.
Received March 30, 2012. Accepted May 2, 2012.
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